Trade‐offs in carbon‐degrading enzyme activities limit long‐term soil carbon sequestration with biochar addition
ABSTRACT Biochar amendment is one of the most promising agricultural approaches to tackle climate change by enhancing soil carbon (C) sequestration. Microbial‐mediated decomposition processes are fundamental for the fate and persistence of sequestered C in soil, but the underlying mechanisms are unc...
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| Veröffentlicht in: | Biological reviews of the Cambridge Philosophical Society 2023-08, Vol.98 (4), p.1184-1199 |
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| creator | Feng, Jiao Yu, Dailin Sinsabaugh, Robert L. Moorhead, Daryl L. Andersen, Mathias Neumann Smith, Pete Song, Yanting Li, Xinqi Huang, Qiaoyun Liu, Yu‐Rong Chen, Ji |
| description | ABSTRACT
Biochar amendment is one of the most promising agricultural approaches to tackle climate change by enhancing soil carbon (C) sequestration. Microbial‐mediated decomposition processes are fundamental for the fate and persistence of sequestered C in soil, but the underlying mechanisms are uncertain. Here, we synthesise 923 observations regarding the effects of biochar addition (over periods ranging from several weeks to several years) on soil C‐degrading enzyme activities from 130 articles across five continents worldwide. Our results showed that biochar addition increased soil ligninase activity targeting complex phenolic macromolecules by 7.1%, but suppressed cellulase activity degrading simpler polysaccharides by 8.3%. These shifts in enzyme activities explained the most variation of changes in soil C sequestration across a wide range of climatic, edaphic and experimental conditions, with biochar‐induced shift in ligninase:cellulase ratio correlating negatively with soil C sequestration. Specifically, short‐term ( |
| doi_str_mv | 10.1111/brv.12949 |
| format | Article |
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Biochar amendment is one of the most promising agricultural approaches to tackle climate change by enhancing soil carbon (C) sequestration. Microbial‐mediated decomposition processes are fundamental for the fate and persistence of sequestered C in soil, but the underlying mechanisms are uncertain. Here, we synthesise 923 observations regarding the effects of biochar addition (over periods ranging from several weeks to several years) on soil C‐degrading enzyme activities from 130 articles across five continents worldwide. Our results showed that biochar addition increased soil ligninase activity targeting complex phenolic macromolecules by 7.1%, but suppressed cellulase activity degrading simpler polysaccharides by 8.3%. These shifts in enzyme activities explained the most variation of changes in soil C sequestration across a wide range of climatic, edaphic and experimental conditions, with biochar‐induced shift in ligninase:cellulase ratio correlating negatively with soil C sequestration. Specifically, short‐term (<1 year) biochar addition significantly reduced cellulase activity by 4.6% and enhanced soil organic C sequestration by 87.5%, whereas no significant responses were observed for ligninase activity and ligninase:cellulase ratio. However, long‐term (≥1 year) biochar addition significantly enhanced ligninase activity by 5.2% and ligninase:cellulase ratio by 36.1%, leading to a smaller increase in soil organic C sequestration (25.1%). These results suggest that shifts in enzyme activities increased ligninase:cellulase ratio with time after biochar addition, limiting long‐term soil C sequestration with biochar addition. Our work provides novel evidence to explain the diminished soil C sequestration with long‐term biochar addition and suggests that earlier studies may have overestimated soil C sequestration with biochar addition by failing to consider the physiological acclimation of soil microorganisms over time.</description><identifier>ISSN: 1464-7931</identifier><identifier>EISSN: 1469-185X</identifier><identifier>DOI: 10.1111/brv.12949</identifier><identifier>PMID: 36914985</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Acclimation ; Acclimatization ; biochar addition ; Carbon ; Carbon Sequestration ; Cellulase ; Cellulases ; Charcoal ; Climate change ; Degradation ; Enzymatic activity ; enzyme activity ; Enzymes ; experimental duration ; Ligninase ; Macromolecules ; Meta-analysis ; Microorganisms ; Organic soils ; Phenolic compounds ; Phenols ; Polysaccharides ; Saccharides ; Soil ; Soil amendment ; soil carbon sequestration ; soil microorganism ; Soil microorganisms ; Soils</subject><ispartof>Biological reviews of the Cambridge Philosophical Society, 2023-08, Vol.98 (4), p.1184-1199</ispartof><rights>2023 The Authors. published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.</rights><rights>2023 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3889-babec0c5cf9f935469e917b9f05d4fb74f4b48c479fce5795896833e45082d623</citedby><cites>FETCH-LOGICAL-c3889-babec0c5cf9f935469e917b9f05d4fb74f4b48c479fce5795896833e45082d623</cites><orcidid>0000-0001-7026-6312</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fbrv.12949$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fbrv.12949$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,777,781,1413,27906,27907,45556,45557</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36914985$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Feng, Jiao</creatorcontrib><creatorcontrib>Yu, Dailin</creatorcontrib><creatorcontrib>Sinsabaugh, Robert L.</creatorcontrib><creatorcontrib>Moorhead, Daryl L.</creatorcontrib><creatorcontrib>Andersen, Mathias Neumann</creatorcontrib><creatorcontrib>Smith, Pete</creatorcontrib><creatorcontrib>Song, Yanting</creatorcontrib><creatorcontrib>Li, Xinqi</creatorcontrib><creatorcontrib>Huang, Qiaoyun</creatorcontrib><creatorcontrib>Liu, Yu‐Rong</creatorcontrib><creatorcontrib>Chen, Ji</creatorcontrib><title>Trade‐offs in carbon‐degrading enzyme activities limit long‐term soil carbon sequestration with biochar addition</title><title>Biological reviews of the Cambridge Philosophical Society</title><addtitle>Biol Rev Camb Philos Soc</addtitle><description>ABSTRACT
Biochar amendment is one of the most promising agricultural approaches to tackle climate change by enhancing soil carbon (C) sequestration. Microbial‐mediated decomposition processes are fundamental for the fate and persistence of sequestered C in soil, but the underlying mechanisms are uncertain. Here, we synthesise 923 observations regarding the effects of biochar addition (over periods ranging from several weeks to several years) on soil C‐degrading enzyme activities from 130 articles across five continents worldwide. Our results showed that biochar addition increased soil ligninase activity targeting complex phenolic macromolecules by 7.1%, but suppressed cellulase activity degrading simpler polysaccharides by 8.3%. These shifts in enzyme activities explained the most variation of changes in soil C sequestration across a wide range of climatic, edaphic and experimental conditions, with biochar‐induced shift in ligninase:cellulase ratio correlating negatively with soil C sequestration. Specifically, short‐term (<1 year) biochar addition significantly reduced cellulase activity by 4.6% and enhanced soil organic C sequestration by 87.5%, whereas no significant responses were observed for ligninase activity and ligninase:cellulase ratio. However, long‐term (≥1 year) biochar addition significantly enhanced ligninase activity by 5.2% and ligninase:cellulase ratio by 36.1%, leading to a smaller increase in soil organic C sequestration (25.1%). These results suggest that shifts in enzyme activities increased ligninase:cellulase ratio with time after biochar addition, limiting long‐term soil C sequestration with biochar addition. Our work provides novel evidence to explain the diminished soil C sequestration with long‐term biochar addition and suggests that earlier studies may have overestimated soil C sequestration with biochar addition by failing to consider the physiological acclimation of soil microorganisms over time.</description><subject>Acclimation</subject><subject>Acclimatization</subject><subject>biochar addition</subject><subject>Carbon</subject><subject>Carbon Sequestration</subject><subject>Cellulase</subject><subject>Cellulases</subject><subject>Charcoal</subject><subject>Climate change</subject><subject>Degradation</subject><subject>Enzymatic activity</subject><subject>enzyme activity</subject><subject>Enzymes</subject><subject>experimental duration</subject><subject>Ligninase</subject><subject>Macromolecules</subject><subject>Meta-analysis</subject><subject>Microorganisms</subject><subject>Organic soils</subject><subject>Phenolic compounds</subject><subject>Phenols</subject><subject>Polysaccharides</subject><subject>Saccharides</subject><subject>Soil</subject><subject>Soil amendment</subject><subject>soil carbon sequestration</subject><subject>soil microorganism</subject><subject>Soil microorganisms</subject><subject>Soils</subject><issn>1464-7931</issn><issn>1469-185X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kdFOHCEUhompqbr2whdoSHpTL0Zhhhng0hqtJpuYGG16R4A5rJiZQWF2zXrlI_QZ-yTF3a0XJnJz4Ofjzzn8CB1QckTzOjZxcURLyeQW2qWskQUV9e9Pqz0ruKzoDtpL6Z6QLDTVZ7RTNZIyKepdtLiJuoW_L3-Ccwn7AVsdTRiy0MIsX_lhhmF4XvaAtR39wo8eEu5870fchWGWwRFij1Pw3eYtTvA4hzRGPfp8evLjHTY-2DsdsW5b_6ruo22nuwRfNnWCbs_Pbk4viunVz8vTk2lhKyFkYbQBS2xtnXSyqvNoICk30pG6Zc5w5phhwjIunYWay1rIRlQVsJqIsm3KaoK-r30fYlg1pXqfLHSdHiDMkyq5aAQlDecZ_fYOvQ_zOOTuVJk9BS9pQzJ1uKZsDClFcOoh-l7HpaJEvYahchhqFUZmv24c56aH9o38__sZOF4DT76D5cdO6sf1r7XlP8oPmDc</recordid><startdate>202308</startdate><enddate>202308</enddate><creator>Feng, Jiao</creator><creator>Yu, Dailin</creator><creator>Sinsabaugh, Robert L.</creator><creator>Moorhead, Daryl L.</creator><creator>Andersen, Mathias Neumann</creator><creator>Smith, Pete</creator><creator>Song, Yanting</creator><creator>Li, Xinqi</creator><creator>Huang, Qiaoyun</creator><creator>Liu, Yu‐Rong</creator><creator>Chen, Ji</creator><general>Blackwell Publishing Ltd</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>C1K</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7026-6312</orcidid></search><sort><creationdate>202308</creationdate><title>Trade‐offs in carbon‐degrading enzyme activities limit long‐term soil carbon sequestration with biochar addition</title><author>Feng, Jiao ; Yu, Dailin ; Sinsabaugh, Robert L. ; Moorhead, Daryl L. ; Andersen, Mathias Neumann ; Smith, Pete ; Song, Yanting ; Li, Xinqi ; Huang, Qiaoyun ; Liu, Yu‐Rong ; Chen, Ji</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3889-babec0c5cf9f935469e917b9f05d4fb74f4b48c479fce5795896833e45082d623</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Acclimation</topic><topic>Acclimatization</topic><topic>biochar addition</topic><topic>Carbon</topic><topic>Carbon Sequestration</topic><topic>Cellulase</topic><topic>Cellulases</topic><topic>Charcoal</topic><topic>Climate change</topic><topic>Degradation</topic><topic>Enzymatic activity</topic><topic>enzyme activity</topic><topic>Enzymes</topic><topic>experimental duration</topic><topic>Ligninase</topic><topic>Macromolecules</topic><topic>Meta-analysis</topic><topic>Microorganisms</topic><topic>Organic soils</topic><topic>Phenolic compounds</topic><topic>Phenols</topic><topic>Polysaccharides</topic><topic>Saccharides</topic><topic>Soil</topic><topic>Soil amendment</topic><topic>soil carbon sequestration</topic><topic>soil microorganism</topic><topic>Soil microorganisms</topic><topic>Soils</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Feng, Jiao</creatorcontrib><creatorcontrib>Yu, Dailin</creatorcontrib><creatorcontrib>Sinsabaugh, Robert L.</creatorcontrib><creatorcontrib>Moorhead, Daryl L.</creatorcontrib><creatorcontrib>Andersen, Mathias Neumann</creatorcontrib><creatorcontrib>Smith, Pete</creatorcontrib><creatorcontrib>Song, Yanting</creatorcontrib><creatorcontrib>Li, Xinqi</creatorcontrib><creatorcontrib>Huang, Qiaoyun</creatorcontrib><creatorcontrib>Liu, Yu‐Rong</creatorcontrib><creatorcontrib>Chen, Ji</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Online Library Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environmental Sciences and Pollution Management</collection><collection>MEDLINE - Academic</collection><jtitle>Biological reviews of the Cambridge Philosophical Society</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Feng, Jiao</au><au>Yu, Dailin</au><au>Sinsabaugh, Robert L.</au><au>Moorhead, Daryl L.</au><au>Andersen, Mathias Neumann</au><au>Smith, Pete</au><au>Song, Yanting</au><au>Li, Xinqi</au><au>Huang, Qiaoyun</au><au>Liu, Yu‐Rong</au><au>Chen, Ji</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Trade‐offs in carbon‐degrading enzyme activities limit long‐term soil carbon sequestration with biochar addition</atitle><jtitle>Biological reviews of the Cambridge Philosophical Society</jtitle><addtitle>Biol Rev Camb Philos Soc</addtitle><date>2023-08</date><risdate>2023</risdate><volume>98</volume><issue>4</issue><spage>1184</spage><epage>1199</epage><pages>1184-1199</pages><issn>1464-7931</issn><eissn>1469-185X</eissn><abstract>ABSTRACT
Biochar amendment is one of the most promising agricultural approaches to tackle climate change by enhancing soil carbon (C) sequestration. Microbial‐mediated decomposition processes are fundamental for the fate and persistence of sequestered C in soil, but the underlying mechanisms are uncertain. Here, we synthesise 923 observations regarding the effects of biochar addition (over periods ranging from several weeks to several years) on soil C‐degrading enzyme activities from 130 articles across five continents worldwide. Our results showed that biochar addition increased soil ligninase activity targeting complex phenolic macromolecules by 7.1%, but suppressed cellulase activity degrading simpler polysaccharides by 8.3%. These shifts in enzyme activities explained the most variation of changes in soil C sequestration across a wide range of climatic, edaphic and experimental conditions, with biochar‐induced shift in ligninase:cellulase ratio correlating negatively with soil C sequestration. Specifically, short‐term (<1 year) biochar addition significantly reduced cellulase activity by 4.6% and enhanced soil organic C sequestration by 87.5%, whereas no significant responses were observed for ligninase activity and ligninase:cellulase ratio. However, long‐term (≥1 year) biochar addition significantly enhanced ligninase activity by 5.2% and ligninase:cellulase ratio by 36.1%, leading to a smaller increase in soil organic C sequestration (25.1%). These results suggest that shifts in enzyme activities increased ligninase:cellulase ratio with time after biochar addition, limiting long‐term soil C sequestration with biochar addition. Our work provides novel evidence to explain the diminished soil C sequestration with long‐term biochar addition and suggests that earlier studies may have overestimated soil C sequestration with biochar addition by failing to consider the physiological acclimation of soil microorganisms over time.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>36914985</pmid><doi>10.1111/brv.12949</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-7026-6312</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Acclimation Acclimatization biochar addition Carbon Carbon Sequestration Cellulase Cellulases Charcoal Climate change Degradation Enzymatic activity enzyme activity Enzymes experimental duration Ligninase Macromolecules Meta-analysis Microorganisms Organic soils Phenolic compounds Phenols Polysaccharides Saccharides Soil Soil amendment soil carbon sequestration soil microorganism Soil microorganisms Soils |
| title | Trade‐offs in carbon‐degrading enzyme activities limit long‐term soil carbon sequestration with biochar addition |
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